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Management of the severely malnourished child:


perspective from developing countries
Maharaj K Bhan, Nita Bhandari and Rajiv Bahl
BMJ 2003;326;146-151
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Clinical review

Management of the severely malnourished child:


perspective from developing countries
Maharaj K Bhan, Nita Bhandari, Rajiv Bahl
Careful assessment and appropriate treatment and rehabilitation using standard protocols that are
easy to follow reduce morbidity and mortality

Department of
Paediatrics, All
India Institute of
Medical Sciences,
Ansari Nagar, New
Delhi-110029, India
Maharaj K Bhan
professor
Nita Bhandari
scientist
Rajiv Bahl
scientist
Correspondence to:
M K Bhan
community.research@
cih.uib.no
BMJ 2003;326:14651

In the 1990s, the number of underweight children in


developing countries declined from 177 million to 149
million.1 The incidence of severe malnutrition also
declined but, despite this, severe malnutrition remains
an important problem (fig 1).2 3 In India, for example,
2.8% of children under 5 are severely wasted.3
Malnutrition is a contributing factor in nearly 60% of
deaths in children for which infectious disease is an
underlying cause.4 Malnutrition is also linked to an
increased risk of death in children with diarrhoea and
acute infections of the lower respiratory system and it
may be linked to malariaand possibly measlestoo.5
Death rates caused by severe malnutrition have
changed little over the past few decades in hospitals of
developing countries (median 23.5% during the 1990s)
because malnutrition was inappropriately managed.6
Recent studies from Bangladesh and Brazil, however,
have reported a substantial decline in case fatality after
the adoption of new treatment protocols by hospitals.7 8 This review describes the new treatment
regimens that have been introduced and the evidence
that justifies their use.9

We performed a Medline search for the past 10 years


and a Cochrane database search; we also sourced publications of the World Health Organization that were
related to malnutrition. The search string used was
Children under 3 years (%)

The high case fatality rates in children with severe


malnutrition can be substantially reduced by
adopting standardised treatment protocols
Children with weight for height below 70% of the
National Centre for Health Statistics median,
bipedal oedema, or visible severe wasting should
be hospitalised for initial stabilisation and
preferably until full recovery
In severely malnourished children with diarrhoea,
intravenous fluids should be restricted to patients
showing signs of shock; other severely
malnourished children should be given an oral
rehydration salts solution with a lower sodium
concentration and a higher potassium
concentration than the standard WHO
rehydration salts solution
Prevention and prompt treatment of
hypoglycaemia and hypothermia reduce case
fatality

Sources and selection criteria

100

Summary points

Severely malnourished children require


supplements (up to twice the recommended daily
allowance) of vitamins, potassium, magnesium,
zinc, copper, selenium, and iodine. Iron should be
given only after the childs appetite has returned

NFHS-1 (1992-3)3

90

NFHS-2 (1998-9)4

80
70
60

During the initial week of treatment, only 330-420


kJ/kg energy and 1-1.5 g/kg protein should be
given, to avoid metabolic stress
During rehabilitation, intakes of energy and
protein should be gradually increased to
630-920 kJ/kg/day and 4-5 g/kg/day,
respectively, to achieve a weight gain of
> 10 g/kg/day until recovery

50
40
30
20
10
0

Underweight

Stunted

Wasted

Fig 1 Percentage of undernourished children in India during the


1990s. NFHS=national family health survey

146

malnutrition or protein energy malnutrition not obesity, and we identified 4818 references. We briefly
reviewed references that were related to assessment,
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pathophysiology, and treatment of severe malnutrition
in children to assess their relevance. We excluded
references related to malnutrition in adults, secondary
malnutrition, case series or case reports, and
uncontrolled intervention trials. We reviewed the
remaining 140 studies in detail.

Identification of children with severe


malnutrition
An appropriate definition of severe malnutrition
should enable the identification of children at high risk
of death. In a study of 1202 children in a Kenyan hospital, bipedal oedema (indicating kwashiorkor) and two
marasmus indicatorsvisible severe wasting and a
weight for height z score of < -3 (more than three
standard deviation units below the median of the international reference population) were associated with
three to four times the risk of mortality.10 WHO has
recommended using these three criteria as the best
way to identify children with severe malnutrition.9
A low cut off z score ( < -4.4) for weight for age was
not associated with an increased risk of mortality.10 This
may be because low weight for age is largely the result of
low height in populations where stunting is prevalent
and severe. Weight for height rather than weight for age
is a better indicator of recent or ongoing weight loss or
wasting.11 Visible severe wasting may be used to identify
severe malnutrition when height can not be measured9;
it can be recognised by muscle wasting, especially in the
gluteal region; loss of subcutaneous fat; and prominence
of bony structures, particularly over the thorax.
In community based studies, mid-upper arm
circumference was a good predictor of child mortality
but the performance varied by age.12 When a fixed cut
off was used, wasting was overdiagnosed among younger
children and underdiagnosed among older ones.12

Assessment of severely malnourished


children
Clinical assessment of severely malnourished children
is difficult, especially with respect to assessing how
dehydrated they are. Dehydration is currently classified
as none, some, and severe.9 In severely malnourished children, distinguishing between some dehydration and severe dehydration is difficult. Practically,
dehydration is considered to be severe if the child
shows signs of shock and lethargy or loss of consciousness; all other severely malnourished children with
acute watery diarrhoea may be assumed to have
some dehydration.9 13
Diagnosing severe infection is equally difficult
because the usual signssuch as feverare often
absent. Severe infection is indicated if the child has
hypothermia, hypoglycaemia, or lethargy, is unable to
breastfeed, or looks sick. Recent intake of food and
fluid and the degree of anorexia need to be assessed
for planning feeding regimens. Blood glucose should
be measured (by Dextrostix or biochemical analysis)
routinely. If this is not possible, the children should be
treated as if they have hypoglycaemia. If they have
severe palmar pallor, haemoglobin or haematocrit
estimation is indicated to assess the need for blood
transfusion. A child with haemoglobin < 4 g/dl or
haemoglobin 4-6 g/dl with respiratory distress
indicates the need for blood transfusion.9
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Routine microscopic examination and culture of


urine should be performed because urinary tract infections are common.14 Chest radiograph and Mantoux
test are indicated if the child has had contact with a
person with tuberculosis, has poor growth despite
good food intake, has a history of chronic cough
(longer than 30 days), or has a chest infection that fails
to respond to antibiotics. The results of the Mantoux
test may be falsely negative in severe malnutrition.
Samples of stomach fluids obtained by aspiration on
three consecutive early mornings should be sent for
microscopic examination. Stool examination for
giardiasis is indicated if there is poor weight gain
despite good food intake.

Management of severely malnourished


children
Severely malnourished children should be managed in
hospital during the acute and rehabilitation phases.9
Shorter stays in hospital for initial stabilisation followed
by domiciliary care may, however, be equally effective. In
a study in Bangladesh, case fatality of severely malnourished children treated in hospital till they recovered and
of children rehabilitated through day care or at home
after a week of hospitalisation was similar ( < 5%).15 The
latter approach was less costly, but the results were
obtained in a carefully selected group and therefore may
not represent the wider population. Home based
regimens may result in only partial recovery.16
All severely malnourished children should ideally
receive initial treatment in treatment centres and once
they gain weight, they should be selected for early discharge according to carefully defined criteria.

General principles of treatment


Treatment involves stabilisation for the first seven days
and rehabilitation over the following five weeks (fig 2).9
Severe malnutrition leads to profound metabolic and
physiological changes and reduces the functional
capacity of the heart, liver, kidneys, and gastrointestinal

Acute or stabilisation phase

Rehabilitation phase

Week 1

Week 26

Day 12

Day 37

Look for and treat


Hypoglycaemia
Hypothermia
Dehydration
Infection

Specific treatment for all children


Electrolytes
Micronutrients

No iron

With iron

Sensory stimulation
Initial feeding
Feeding to achieve catch-up growth

Fig 2 Time frame for individual components of management of a child with severe
malnutrition

147

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Box 1: Fluid treatment for a child with severe malnutrition and


diarrhoea9
If the child is showing signs of shock and is lethargic or unconscious, give
any of the following solutions: intravenous Ringers lactate with 5% glucose,
half normal saline with 5% glucose, or half strength Darrows solution with
5% glucose. If these solutions are not available, use Ringers lactate
Treatment regimen: 15 ml/kg intravenous fluid to be given over 1 hour.
Repeat if the child improves. If the child fails to improve, consider septic
shock
If the child has no signs of shock and is passing several watery stools,
assume some dehydration and use oral rehydration salts solution with
reduced osmolarity and added potassium, or ReSoMal, for rehydration
Treatment regimen: 5 ml/kg every 30 minutes for the first 2 hours; 5
ml/kg/hour for the next 4-10 hours

Table 1 Preparation of ReSoMal, one type of rehydration


solution for severely malnourished children9
Ingredients

Amount

Water
WHO oral rehydration salts solution*

2 litre
One 1 litre packet

Sucrose

50 g

Electrolyte-mineral solution

40 ml

*3.5 g sodium chloride, 2.9 g trisodium citrate dihydrate, 1.5 g potassium


chloride, 20 g glucose.
See table 3 for the recipe. If the solution cannot be prepared, use 45 ml of
KCl solution (100 g KCl in 1 litre of water) instead.

tract.13 Too much food, particularly protein, in the


initial phase aggravates the metabolic imbalance. As
appetite returns, intakes of energy and protein are
increased so that the shortfall in the growth of the
patient can be made up.

Stabilisation or acute phase


Correction of shock and dehydration
Intravenous fluids should be restricted to patients with
signs of shock; all other children with dehydration
should be treated with oral rehydration salts solution.9 13 An oral rehydration salts solution with reduced
osmolarity75 mmol/l sodium, 20 mmol/l potassium,
and 75 mmol/l glucoseis now recommended universally to treat dehydration because it reduces stool output, the duration of diarrhoea, and the need for
unscheduled intravenous fluids when compared with
the WHO oral rehydration salts solution.17 Some
experts believe that the sodium concentration of oral
rehydration salts solution for severely malnourished
children should be even lower (45-60 mmol/l) because

high intakes of sodium may cause heart failure,


especially in children with oedema.18
A special oral rehydration salts solution for severely
malnourished children, ReSoMal, used initially in refugee camps, has been endorsed by the WHO. It contains
45 mmol/l sodium, 40 mmol/l potassium, and magnesium, zinc, copper, and sucrose to prevent hypoglycaemia and make the solution isotonic. This formulation
has not yet been evaluated in randomised controlled
trials (table 1).9 Oral rehydration salts solution with
reduced osmolarity and extra potassium should soon
be universally available (box 1).
Other life threatening complications
Two other common complications, hypoglycaemia and
hypothermia, which often occur together, are signs of
possible serious infection and are associated with a
high case fatality.19 Body temperature has been shown
to decrease during hypoglycaemia.20 Rectal temperature less than 35.5C or axillary temperature less than
35C indicates hypothermia.9 Treatment includes
prompt initiation of two hourly feeding (day and
night); keeping the child well clothed, with the head
covered, in a warm environment; and antibiotics for
infection, which is likely to be present.
Testing for hypoglycaemia (glucose < 54 mg/dl)
should be done routinely using Dextrostix. If the test
results are positive, 50 ml of 10% glucose or sucrose
solution should be given orally or by nasogastric tube
followed by feeding as soon as possible.9 If the child is
unconscious, 5 ml/kg of 10% glucose should be given
intravenously or by nasogastric tube. Blood sugar
should be checked after 30 minutes and, if low, more
10% glucose solution should be given. If the rectal
temperature falls below 35.5C, or if there is deterioration in the level of consciousness, measurement with
Dextrostix should be repeated and treatment provided
accordingly.

Treatment of infections
No randomised controlled trials comparing empirical
antibiotic treatment with selective antibiotic treatment
have been undertaken. Although severely malnourished children may not have obvious signs of infection
such as fever and tachypnoea, the prevalence of bacteraemia, urinary tract infections, and pneumonia is
high.21 This high prevalence justifies empirical antibiotic treatment. WHO recommends using such treatment for the first seven days. Intravenous antibiotics
are recommended if hypothermia or hypoglycaemia is
present or if the child is lethargic or appears very ill.9
The guidelines proposed by Stegen et al for initiating
antituberculosis treatment may be used.22

Electrolyte imbalance

A severely malnourished child

148

Most severely malnourished children have deficiencies


in potassium and magnesium, which may take two
weeks or more to correct. Low concentrations of intracellular potassium promote sodium and water
retention, reduce myocardial contractility, and affect
transport of ions across cell membranes.23 Magnesium
deficiency leads to impaired retention of potassium.24
Evidence for the efficacy of potassium and magnesium supplementation from controlled clinical trials is
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limited. In a double blind controlled trial in children
with oedematous severe malnutrition, a total potassium intake of 7.7 mmol/kg/day compared with
4.7 mmol/kg/day during the first week did not significantly reduce mortality during hospitalisation, but
fewer children died after day 5 of hospitalisation.23
Trials of magnesium supplementation have been small
and the results were inconclusive.25 26 WHO recommends that extra potassium and magnesium be added
to feeds during their preparation (3-4 mmol/kg/day
and 0.4-0.6 mmol/kg, respectively).

Table 3 Recipes and composition of starter formulas and


catch-up formula9
Starter
formula with
Catch up
Starter
formula(F-75a*) cereal(F-75b) formulaF-100
Dried skimmed milk (g)
Sugar (g)
Cereal flour (g)
Vegetable oil (g)
Electrolyte-mineral solution (ml)
Water: use to make up final
solution to (ml)

25

25

80

100

70

50

35

27

27

60

20

20

20

1000

1000

1000

314

314

418

Contents per 100 ml

Micronutrient deficiencies

Energy (kJ)

Severely malnourished children are often deficient in


vitamin A, zinc, iron, folic acid, copper, and selenium.
Deficiencies in zinc and vitamin A impair the function
of the immune system and have direct effects on the
structure and function of mucosa.27 Copper deficiency
is characterised by neutropenia, bone abnormalities,
and microcytic anaemia that fails to respond to iron.28
Cardiac function is impaired in selenium deficiency.29
Zinc supplementation reduces the incidence of diarrhoea and pneumonia and improves growth.30 Vitamin
A supplementation has been shown to reduce mortality
and morbidity due to diarrhoea and measles.31 Iron supplementation improves cognition and growth but is not
recommended in the acute phase because it may worsen
existing infection.32 33 Trials of copper supplementation
in severely malnourished children show inconsistent
results.34 35 Selenium supplementation has not been
assessed in controlled trials.
Table 2 Composition of electrolyte-mineral solution* for severely
malnourished children9
Ingredient

Mass(g)

Potassium chloride (KCl)

224

mmol per 20 ml
24

Tripotassium citrate

81

Magnesium chloride (MgCl2.6H20)

76

Zinc acetate (Zn accetate.2H20)

8.2

0.3

Copper sulphate (CuSO4.5H20)

1.4

0.045

*To be added to diet or oral rehydration salts solution.


Use water to make up to 2.5 l. If available, also add selenium (0.028 g of
sodium selenate, NaSe4.10H20) and iodine (0.012 g of potassium iodide, KI) per
2.5 l. Add 20 ml of the solution to a litre of diet or oral rehydration salts
solution.

Giving micronutrients to patients is often difficult


because suitable formulations are not available. One
approach is to prepare an electrolyte-mineral solution
(table 2).9 To mask the taste, the solution can be added
to food. An alternative approach is to give multivitamin
supplements: folic acid (5 mg on day 1, then 1
mg/day); zinc as acetate, sulphate, or gluconate (2 mg
elemental zinc/kg/day); copper (0.3 mg elemental
copper/kg/day); andonce the infant begins to gain
weightferrous sulphate (3 mg elemental iron/kg/
day).9 Daily intake of individual micronutrients should
be up to twice the recommended daily allowance.
Additionally, vitamin A can be given orally (age < 6
months, 50 000 IU; age 6-12 months, 100 000 IU;
older children, 200 000 IU) on day 1.9

Dietary treatment during acute phase


Feeding should be started as soon as possible. Diets
used for initial feeding should have low osmolarity and
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Protein (g)

0.9

1.1

2.9

Lactose (g)

1.3

1.3

4.2

Potassium (mmol)

4.0

4.2

6.3

Sodium (mmol)

0.6

0.6

1.9

Magnesium (mmol)

0.43

0.46

0.73

Zinc (mg)

2.0

2.0

2.3

Copper (mg)

0.25

0.25

% energy from protein

% energy from fat


Osmolality (mOsm/l)

0.25
12

32

32

53

413

334

419

*A comparable initial diet can be made from 35 g whole dried milk, 100 g
sugar, 20 g oil, 20 ml electrolyte-mineral solution (table 3), and water to make
a final volume of 1000 ml. If using fresh cows milk, take 300 ml milk, 100 g
sugar, 20 ml oil, 20 ml electrolyte-mineral solution and water to make 1000 ml.
Cook for 4 minutes. This may be helpful for children with dysentery or
persistent diarrhoea.
A comparable catch-up formula can be made from 110 g whole dried milk,
50 g sugar, 30 g oil, 20 ml electrolyte-mineral solution, and water to make up
to 1000 ml. If using fresh cows milk, take 880 ml milk, 75 g sugar, 20 ml oil,
20 ml electrolyte-mineral solution, and water to make up to 1000 ml.

low lactose and should provide 330-420 kJ/kg energy


and 1-1.5 g/kg protein per day.7 9 The recipe and composition of a milk based starter formula (F-75a) is
shown in table 3. A milk and cereal based formula
(F-75b) has the advantage of lower osmolarity, which
may be particularly beneficial for children with
diarrhoea; however, it needs to be cooked, which may
not always be practical.
The child should be fed every two hoursor, if this
is not possible, every three hoursday and night.
Breastfeeding should be continued. A recommended
feeding schedule is shown in table 4. If the childs
intake does not reach 330 kJ/kg/day despite frequent
feeds, coaxing, and reoffering, the remaining feed
should be given by nasogastric tube.

Rehabilitation phase
The return of the patients appetite heralds the
rehabilitation phase and usually occurs a week after
treatment is started. The goal of treatment then is to
achieve a weight gain greater than 10 g/kg/day until
the patient has fully recovered (box 2). Frequent feeds,
unlimited in amount, help to achieve daily energy and
protein intakes of 630-920 kJ/kg/day and 4-5
g/kg/day, respectively. Increases in energy and protein
intake should be gradual to avoid cardiac failure. A
Table 4 Recommended feeding schedule9
Frequency

Volume/kg/feed
(ml)

Volume/kg/day
(ml)

1-2

2 hourly

11

130

3-5

3 hourly

16

130

>6

4 hourly

22

130

Days

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Box 2: Monitoring progress during treatment


If weight gain is good ( > 10 g/kg/day), continue
with the same treatment
If weight gain is moderate (5-10 g/kg/day), check
whether intake targets are being met or if infection has
been overlooked
If weight gain is poor ( < 5 g/kg/day), make a full
assessment and look particularly for inadequate
feeding, untreated infection, tuberculosis, and
psychological problems
A child is considered to have recovered on reaching
a weight for height that is 90% of the National Centre
for Health Statistics median

Box 3: Criteria for discharge before full


recovery9
Age 12 months or older
Antibiotic treatment completed
Good appetite
Good weight gain
No oedema
Potassium, magnesium, mineral supplements, and
vitamin supplements taken for two weeks
Mother or caretaker is not employed outside the
home, has received specific training on appropriate
feeding, has the financial resources to feed the child,
and is motivated to follow the advice given

milk based catch-up formula (F-100) that provides 420


kJ/100 ml and 2.9 g protein/100 ml is appropriate
(table 3). Modified porridges or other complementary
foods can be used as long as they have energy and protein content similar to that provided by F-100.
Porridges prepared with locally available cereals in
milk or other complementary foods that have been
modified to provide energy and protein concentrations
comparable to the F-100 catch-up formula are also

Box 4: Feeding children at home after discharge before full


recovery
Feed at least five times a day
Modify the usual home foods to contain approximately 420 kJ and 2-3
g/kg proteins per 100 g food
Give high energy snacks between meals
Encourage the child to eat
Give food in a separate bowl
Give electrolyte and mineral supplements
Allow breastfeeding as often as the child wants to

Box 5: Important research questions that need to be addressed


Clinical efficacy of magnesium, high dose potassium, copper, and
selenium, including impact on case fatality rates
Clinical evaluation of different oral rehydration salts formulations and
fluid regimens for managing dehydration
Comparison of empirical antibiotic treatment with selective antibiotic
treatment during the initial phase
Comparison of community based rehabilitation with hospital based
rehabilitation

150

acceptable. Breastfeeding should be continued but the


diet should be given first. If weight gain is less than
10 g/kg/day, infection or inadequate intake of energy
and protein are likely to be contributing factors.
Recovery from malnutrition is possible in children
with HIV or AIDS, but it can take longer and treatment
failures are more common.9 36 37 Love and care, a
cheerful stimulating environment, structured play
therapy, progressively increasing physical activity, and
mothers involvement in care of the child are
important components of therapy.9 38
WHO recommends that a child be discharged
from hospital when the weight for height reaches 90%
of the National Centre for Health Statistics median, but
it is unclear whether use of a lower cut off pointfor
example, 80%is linked to poor outcome.9 Discharging patients before they have fully recovered should be
considered only if the criteria in box 3 are met.
If a child is discharged before full recovery, he or
she should be fed at home (see box 4).

Educational resources
World Health Organization, Division of Child Health
and Development. Integrated Management of
Childhood Illness. Geneva: WHO, 1997. (Document
ref WHO/CHD/97.3E) www.who.int/
child-adolescent-health/publications/IMCI/
in_service.htm (accessed 18 Dec 2002).
World Health Organization, Department Child and
Adolescent Health and Development. Management of
the child with a serious infection or severe
malnutrition. Guidelines for care at the first referral
level in developing countries. Geneva: WHO, 2000.
www.who.int/child-adolescent-health/publications/
referral_care/referencepdf/01prelims.pdf (accessed 20
Nov 2002).

Conclusions
The high case fatality rates among severely malnourished children have been reduced by using standardised and easily implementable protocols, and
improved decision making, monitoring and supervision. Admittedly, not all the recommendations are
based on firm evidence and more research is needed
(box 5), but the approach described in this article has
been shown to work. Whether resources should be
focused on promoting optimal growth or on
rehabilitation of the severely malnourished children is
not an issue, as the two approaches are complementary. Effective rehabilitation of the severely malnourished child, an area that has long been neglected, must
now find a key place in strategies to reduce child morbidity and mortality.
Contributors: NB did the search after all three authors had
developed the search strategy. All three authors reviewed the
papers independently. MKB wrote the first draft, which was
revised and restructured by NB and RB. The final draft was
reviewed and approved together by all three authors.
Funding: None.
Competing interests: None declared.
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Lesson of the week


Unsuspected haemophilia in children with a single
swollen joint
Beatrice Nolan, Vicky Vidler, Ajay Vora, Michael Makris
A clotting screen should always be performed in a
child with a swollen joint, even if there is a history of
minor trauma, to exclude underlying bleeding
disorders. A prompt diagnosis of haemophilia will
allow early arrest of bleeding by appropriate treatment,
which will in turn minimise complications and reduce
total exposure to blood products.

Case reports
Case 1
A 1 year old boy, an only child, presented to an
accident and emergency department with a painful,
swollen right elbow following minor trauma. Examination and a radiograph showed no evidence of bone
injury and he was sent home.
Three days later, he was brought back because of
increasing pain and swelling. Joint aspiration yielded
BMJ VOLUME 326

18 JANUARY 2003

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haemorrhagic fluid. Osteomyelitis was suspected and


he was started empirically on antibiotic treatment.
Approximately four weeks later, as the effusion had not
resolved, the joint was explored, yielding dark blood,
and a biopsy specimen was taken from a localised area
of synovitis. Postoperatively the wound bled persistently. A coagulation screen showed normal prothrombin time but prolonged activated partial
thromboplastin time (96 s; normal range 24-35 s)
which was corrected by the addition of normal plasma,
suggesting an underlying factor deficiency; at this stage
he was referred to us at the regional comprehensive
carer haemophilia centre. On further questioning it
was found that his maternal great grandfather had bled
abnormally after minor surgical procedures. His factor
VIII concentration was 0.02 IU/ml (normal range 0.51.5 IU/ml). He was given factor VIII concentrate daily
for 10 days and then three times a week for a further

A clotting screen
to exclude
haemophilia is
an essential
investigation in
a child with a
single swollen
joint
Correspondence to:
M Makris
m.makris@sheffield.
ac.uk
continued over
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